Department of Medical BioSciences, Radboud University Medical Center, Geert Grooteplein 28, 6525 GA, Nijmegen, the Netherlands.
Laboratory of Hematology, Radboud University Medical Center, Geert Grooteplein Zuid 10, 6525 GA, Nijmegen, the Netherlands.
J Leukoc Biol. 2024 Nov 27;116(6):1554-1567. doi: 10.1093/jleuko/qiae164.
Tumor-derived prostaglandin E2 (PGE2) impairs antitumor immunity by priming suppressive functions on various immune cell types, including dendritic cells (DCs). In this way, tumors mediate DC dysfunction and hamper their antitumoral activity. PGE2 is known to modulate DC function via signaling through the E-type prostanoid receptor 2 (EP2) and EP4. Preclinical studies have demonstrated the therapeutic value of targeting EP2/4 receptor signaling in DCs. Ongoing phase 1 clinical trials with EP antagonists have shown immunomodulation in cancer patients. However, the systemic drug administration leads to off-target events and subsequent side effects. To limit the off-target effects of EP targeting, EP2 and EP4 antagonists were encapsulated in polymeric nanoparticles (NPs). In this study, we evaluated the efficacy of EP2/4-specific antagonists encapsulated in NPs to protect conventional type 2 DCs (cDC2s) from suppressive effects of tumor-derived PGE2 in different tumor models. We show that tumor-derived PGE2 signals via EP2/4 to mediate the acquisition of a suppressive phenotype of cDC2s. EP2/4 antagonists encapsulated in NPs impaired the conversion of cDC2s toward a suppressive state and inhibited the occurrence of suppressive features such as interleukin-10 production or the ability to expand regulatory T cells. Importantly, the NPs abolished the transition toward this suppressive state in different tumor models: melanoma-conditioned media, ascites fluid derived from ovarian cancer patients (2-dimensional), and upon coculture with colorectal cancer patient-derived organoids (3-dimensional). We propose that targeting the PGE2-EP2/4 axis using NPs can achieve immunomodulation in the immune system of cancer patients, alleviate tumor-derived suppression, and thus facilitate the development of potent antitumor immunity in cancer patients.
肿瘤衍生的前列腺素 E2(PGE2)通过在各种免疫细胞类型(包括树突状细胞(DCs))上诱导抑制功能来损害抗肿瘤免疫。通过这种方式,肿瘤介导 DC 功能障碍并阻碍其抗肿瘤活性。已知 PGE2 通过 E 型前列腺素受体 2(EP2)和 EP4 的信号传导来调节 DC 功能。临床前研究已经证明了针对 DC 中 EP2/4 受体信号的治疗价值。正在进行的 EP 拮抗剂的 1 期临床试验已显示出癌症患者的免疫调节作用。然而,全身药物给药会导致脱靶事件和随后的副作用。为了限制 EP 靶向的脱靶效应,EP2 和 EP4 拮抗剂被包裹在聚合物纳米颗粒(NPs)中。在这项研究中,我们评估了包裹在 NPs 中的 EP2/4 特异性拮抗剂保护常规 2 型 DC(cDC2)免受肿瘤衍生的 PGE2 在不同肿瘤模型中的抑制作用的功效。我们表明,肿瘤衍生的 PGE2 通过 EP2/4 信号传导来介导 cDC2 获得抑制表型。包裹在 NPs 中的 EP2/4 拮抗剂会损害 cDC2 向抑制状态的转化,并抑制抑制特征的发生,例如白细胞介素-10 的产生或调节性 T 细胞的扩增能力。重要的是,NP 消除了不同肿瘤模型中向这种抑制状态的转变:黑色素瘤条件培养基、卵巢癌患者腹水(2 维)和与结直肠癌患者衍生类器官共培养(3 维)。我们提出,使用 NPs 靶向 PGE2-EP2/4 轴可以在癌症患者的免疫系统中实现免疫调节,减轻肿瘤衍生的抑制作用,从而促进癌症患者产生有效的抗肿瘤免疫。